Investigating tritrophic interactions using bioenergetic demographic models.

A central debate in ecology has been the long-running discussion on the role of apex predators in affecting the abundance and dynamics of their prey. In terrestrial systems, research has primarily relied on correlational approaches, due to the challenge of implementing robust experiments with replication and appropriate controls. A consequence of this is that we largely suffer from a lack of mechanistic understanding of the population dynamics of interacting species, which can be surprisingly complex. Mechanistic models offer an opportunity to examine the causes and consequences of some of this complexity. We present a bioenergetic mechanistic model of a tritrophic system where the primary vegetation resource follows a seasonal growth function, and the herbivore and carnivore species are modeled using two integral projection models (IPMs) with body mass as the phenotypic trait. Within each IPM, the demographic functions are structured according to bioenergetic principles, describing how animals acquire and transform resources into body mass, energy reserves, and breeding potential. We parameterize this model to reproduce the population dynamics of grass, elk, and wolves in northern Yellowstone National Park (USA) and investigate the impact of wolf reintroduction on the system. Our model generated predictions that closely matched the observed population sizes of elk and wolf in Yellowstone prior to and following wolf reintroduction. The introduction of wolves into our basal grass-elk bioenergetic model resulted in a population of 99 wolves and a reduction in elk numbers by 61% (from 14,948 to 5823) at equilibrium. In turn, vegetation biomass increased by approximately 25% in the growing season and more than threefold in the nongrowing season. The addition of wolves to the model caused the elk population to switch from being food-limited to being predator-limited and had a stabilizing effect on elk numbers across different years. Wolf predation also led to a shift in the phenotypic composition of the elk population via a small increase in elk average body mass. Our model represents a novel approach to the study of predator-prey interactions, and demonstrates that explicitly considering and linking bioenergetics, population demography and body mass phenotypes can provide novel insights into the mechanisms behind complex ecosystem processes.

Demographic profiles and environmental drivers of variation relate to individual breeding state in a long-lived trans-oceanic migratory seabird, the Manx shearwater.

Understanding the points in a species breeding cycle when they are most vulnerable to environmental fluctuations is key to understanding interannual demography and guiding effective conservation and management. Seabirds represent one of the most threatened groups of birds in the world, and climate change and severe weather is a prominent and increasing threat to this group. We used a multi-state capture-recapture model to examine how the demographic rates of a long-lived trans-oceanic migrant seabird, the Manx shearwater Puffinus puffinus, are influenced by environmental conditions experienced at different stages of the annual breeding cycle and whether these relationships vary with an individual's breeding state in the previous year (i.e., successful breeder, failed breeder and non-breeder). Our results imply that populations of Manx shearwaters are comprised of individuals with different demographic profiles, whereby more successful reproduction is associated with higher rates of survival and breeding propensity. However, we found that all birds experienced the same negative relationship between rates of survival and wind force during the breeding season, indicating a cost of reproduction (or central place constraint for non-breeders) during years with severe weather conditions. We also found that environmental effects differentially influence the breeding propensity of individuals in different breeding states. This suggests individual spatio-temporal variation in habitat use during the annual cycle, such that climate change could alter the frequency that individuals with different demographic profiles breed thereby driving a complex and less predictable population response. More broadly, our study highlights the importance of considering individual-level factors when examining population demography and predicting how species may respond to climate change.

Investigating the Dynamics of Elk Population Size and Body Mass in a Seasonal Environment Using a Mechanistic Integral Projection Model.

Environmentally mediated changes in body size often underlie population responses to environmental change, yet this is not a universal phenomenon. Understanding when phenotypic change underlies population responses to environmental change is important for obtaining insights and robust predictions of population dynamics in a changing world. We develop a dynamic integral projection model that mechanistically links environmental conditions to demographic rates and phenotypic traits (body size) via changes in resource availability and individual energetics. We apply the model to the northern Yellowstone elk population and explore population responses to changing patterns of seasonality, incorporating the interdependence of growth, demography, and density-dependent processes operating through population feedback on available resources. We found that small changes in body size distributions can have large impacts on population dynamics but need not cause population responses to environmental change. Environmental changes that altered demographic rates directly, via increasing or decreasing resource availability, led to large population impacts in the absence of substantial changes to body size distributions. In contrast, environmentally driven shifts in body size distributions could occur with little consequence for population dynamics when the effect of environmental change on resource availability was small and seasonally restricted and when strong density-dependent processes counteracted expected population responses. These findings highlight that a robust understanding of how associations between body size and demography influence population responses to environmental change will require knowledge of the shape of the relationship between phenotypic distributions and vital rates, the population status with regard to its carrying capacity, and importantly the nature of the environmentally driven change in body size and carrying capacity.

Views of UK doctors in training on the timing of choosing a clinical specialty: quantitative and qualitative analysis of surveys 3 years after graduation.

BACKGROUND: Workforce studies show a declining proportion of UK junior doctors proceeding directly to specialist training, with many taking career breaks. Doctors may be choosing to delay this important career decision. AIM: To assess doctors' views on the timing of choosing a clinical specialty. METHODS: Surveys of two cohorts of UK-trained doctors 3 years after qualification, in 2011 and 2015. RESULTS: Presented with the statement 'I had to choose my career specialty too soon after qualification', 61% agreed (27% strongly) and 22% disagreed (3% strongly disagreed). Doctors least certain about their choice of specialty were most likely to agree (81%), compared with those who were more confident (72%) or were definite regarding their choice of long-term specialty (54%). Doctors not in higher specialist training were more likely to agree with this statement than those who were (72% vs 59%). Graduate medical school entrants (ie, those who had completed prior degrees) were less likely to agree than non-graduates (56% vs 62%). Qualitative analysis of free text comments identified three themes as reasons why doctors felt rushed into choosing their future career: insufficient exposure to a wide range of specialties; a desire for a greater breadth of experience of medicine in general; and inadequate career advice. CONCLUSIONS: Most UK-trained doctors feel rushed into choosing their long-term career specialty. Doctors find this difficult because they lack sufficient medical experience and adequate career advice to make sound choices. Workforce trainers and planners should enable greater flexibility in training pathways and should further improve existing career guidance.

Large-effect loci affect survival in Tasmanian devils (Sarcophilus harrisii) infected with a transmissible cancer.

Identifying the genetic architecture of complex phenotypes is a central goal of modern biology, particularly for disease-related traits. Genome-wide association methods are a classical approach for identifying the genomic basis of variation in disease phenotypes, but such analyses are particularly challenging in natural populations due to sample size difficulties. Extensive mark-recapture data, strong linkage disequilibrium and a lethal transmissible cancer make the Tasmanian devil (Sarcophilus harrisii) an ideal model for such an association study. We used a RAD-capture approach to genotype 624 devils at ~16,000 loci and then used association analyses to assess the heritability of three cancer-related phenotypes: infection case-control (where cases were infected devils and controls were devils that were never infected), age of first infection and survival following infection. The SNP array explained much of the phenotypic variance for female survival (>80%) and female case-control (>61%). We found that a few large-effect SNPs explained much of the variance for female survival (~5 SNPs explained >61% of the total variance), whereas more SNPs (~56) of smaller effect explained less of the variance for female case-control (~23% of the total variance). By contrast, these same SNPs did not account for a significant proportion of phenotypic variance in males, suggesting that the genetic bases of these traits and/or selection differ across sexes. Loci involved with cell adhesion and cell-cycle regulation underlay trait variation, suggesting that the devil immune system is rapidly evolving to recognize and potentially suppress cancer growth through these pathways. Overall, our study provided necessary data for genomics-based conservation and management in Tasmanian devils.

The Certainty of Uncertainty: Potential Sources of Bias and Imprecision in Disease Ecology Studies.

Wildlife diseases have important implications for wildlife and human health, the preservation of biodiversity and the resilience of ecosystems. However, understanding disease dynamics and the impacts of pathogens in wild populations is challenging because these complex systems can rarely, if ever, be observed without error. Uncertainty in disease ecology studies is commonly defined in terms of either heterogeneity in detectability (due to variation in the probability of encountering, capturing, or detecting individuals in their natural habitat) or uncertainty in disease state assignment (due to misclassification errors or incomplete information). In reality, however, uncertainty in disease ecology studies extends beyond these components of observation error and can arise from multiple varied processes, each of which can lead to bias and a lack of precision in parameter estimates. Here, we present an inventory of the sources of potential uncertainty in studies that attempt to quantify disease-relevant parameters from wild populations (e.g., prevalence, incidence, transmission rates, force of infection, risk of infection, persistence times, and disease-induced impacts). We show that uncertainty can arise via processes pertaining to aspects of the disease system, the study design, the methods used to study the system, and the state of knowledge of the system, and that uncertainties generated via one process can propagate through to others because of interactions between the numerous biological, methodological and environmental factors at play. We show that many of these sources of uncertainty may not be immediately apparent to researchers (for example, unidentified crypticity among vectors, hosts or pathogens, a mismatch between the temporal scale of sampling and disease dynamics, demographic or social misclassification), and thus have received comparatively little consideration in the literature to date. Finally, we discuss the type of bias or imprecision introduced by these varied sources of uncertainty and briefly present appropriate sampling and analytical methods to account for, or minimise, their influence on estimates of disease-relevant parameters. This review should assist researchers and practitioners to navigate the pitfalls of uncertainty in wildlife disease ecology studies.

Factors influencing the decisions of senior UK doctors to retire or remain in medicine: national surveys of the UK-trained medical graduates of 1974 and 1977.

OBJECTIVE: To report attitudes to retirement of late-career doctors. DESIGN: Questionnaires sent in 2014 to all UK medical graduates of 1974 and 1977. SETTING: United Kingdom. PARTICIPANTS: 3695 medical graduates. MAIN OUTCOME MEASURES: Factors which influenced doctors' decisions to retire and factors which encouraged doctors to remain in work. RESULTS: The response rate was 85% (3695/4369). 55% of respondents overall were still working in medicine (whether they had not retired or had retired and returned; 61% of men, 43% of women). Of the retirees, 67% retired when they had originally planned to, and 28% had changed their retirement plans. Fifty per cent of retired doctors cited 'increased time for leisure/other interests' as a reason; 43% cited 'pressure of work'. Women (21%) were more likely than men (11%) to retire for family reasons. Women (27%) were more likely than men (9%) to retire because of the retirement of their spouse. General practitioners (GPs) were more likely than doctors in other specialties to cite 'pressure of work'. Anaesthetists and GPs were more likely than doctors in other specialties to cite the 'possibility of deteriorating skill/competence'. Radiologists, surgeons, obstetricians and gynaecologists, and anaesthetists were most likely to cite 'not wanting to do out-of-hours work'.Doctors who were still working were asked what would encourage them to stay in medicine for longer. Factors cited most frequently were 'reduced impact of work-related bureaucracy' (cited by 45%) and 'workload reduction/shorter hours' (42%). Men (30%) were more motivated than women (20%) by 'financial incentivisation'. Surgeons were most motivated by 'reduction of on-call or emergency commitments'. CONCLUSIONS: Retention policy should address ways of optimising the clinical contribution of senior doctors while offering reduced workloads in the areas of bureaucracy and working hours, particularly in respect of emergency commitments.

Factors associated with less-than-full-time working in medical practice: results of surveys of five cohorts of UK doctors, 10 years after graduation.

BACKGROUND: The greater participation of women in medicine in recent years, and recent trends showing that doctors of both sexes work fewer hours than in the past, present challenges for medical workforce planning. In this study, we provide a detailed analysis of the characteristics of doctors who choose to work less-than-full-time (LTFT). We aimed to determine the influence of these characteristics on the probability of working LTFT. METHODS: We used data on working patterns obtained from long-term surveys of 10,866 UK-trained doctors. We analysed working patterns at 10 years post-graduation for doctors of five graduating cohorts, 1993, 1996, 1999, 2000 and 2002 (i.e. in the years 2003, 2006, 2009, 2010 and 2012, respectively). We used multivariable binary logistic regression models to examine the influence of a number of personal and professional characteristics on the likelihood of working LTFT in male and female doctors. RESULTS: Across all cohorts, 42 % of women and 7 % of men worked LTFT. For female doctors, having children significantly increased the likelihood of working LTFT, with greater effects observed for greater numbers of children and for female doctors in non-primary care specialties (non-GPs). While >40 % of female GPs with children worked LTFT, only 10 % of female surgeons with children did so. Conversely, the presence of children had no effect on male working patterns. Living with a partner increased the odds of LTFT working in women doctors, but decreased the odds of LTFT working in men (independently of children). Women without children were no more likely to work LTFT than were men (with or without children). For both women and men, the highest rates of LTFT working were observed among GPs (~10 and 6 times greater than non-GPs, respectively), and among those not in training or senior positions. CONCLUSIONS: Family circumstances (children and partner status) affect the working patterns of women and men differently, but both sexes respond similarly to the constraints of their clinical specialty and seniority. Thus, although women doctors comprise the bulk of LTFT workers, gender is just one of several determinants of doctors' working patterns, and wanting to work LTFT is evidently not solely an issue for working mothers.

Associations between perceived institutional support, job enjoyment, and intentions to work in the United Kingdom: national questionnaire survey of first year doctors.

BACKGROUND: Identifying factors that improve job satisfaction of new doctors and ease the difficult transition from student to doctor is of great interest to public health agencies. Studies to date have focused primarily on the value of changes to medical school curricula and induction processes in this regard, but have overlooked the extent to which institutional support can influence new doctors' enjoyment of and attitude to work. Here, we examine variation in the perceived level of support received by new medical graduates in the United Kingdom (UK) from their employer and whether this influences enjoyment of and attitudes to the first postgraduate year, and whether doctors who perceived a lower level of support were less inclined to intend a long term career in medicine in the UK. METHODS: All UK medical graduates of 2012 were surveyed in 2013 in a cross-sectional study, towards the end of their first post-graduate year (the 'F1' year of the 2-year Foundation Training Programme for new UK doctors). We used linear regression to assess whether the level of support doctors reported receiving from their employing Trust (Very Good, Good, Adequate, Poor, or Very Poor) was associated with the extent to which they enjoyed their F1 year. Similarly, we assessed the strength of associations between self-reported level of Trust support and doctors' responses to 12 statements about fundamental aspects of their working lives, each assessed on a 5-point scale of agreement. Using χ (2) tests we examined whether doctors' intentions to practise medicine in the UK varied with the level of support they reported receiving from their Trust. RESULTS: The response rate was 45 % (2324/5171). Of 2324 responding junior doctors, 63.8 % reported receiving 'Very Good' (23.6 %) or 'Good' (40.2 %) initial support from their Trust, while a further 27.4 % stated they received 'Adequate' support. 'Poor' support was reported by 5.8 % and 'Very Poor' support by 2.2 %. We found very strong positive associations between the institutional support doctors reported receiving and their enjoyment of the F1 year and their self-expressed attitudes to aspects of their first year of work. Crucially, doctors who reported receiving lower levels of support ('Poor' or 'Very Poor') were significantly less likely to express intentions to continue practising medicine in the UK. CONCLUSIONS: The provision of effective institutional support for graduate doctors may promote workplace satisfaction and could help safeguard the long-term retention of junior doctors.

Self-reported preparedness for clinical work has increased among recent cohorts of UK-trained first-year doctors.

INTRODUCTION: UK medical schools have made considerable efforts to ensure that graduates are well prepared for their first year of clinical work. We report the views of two recent cohorts of UK-trained doctors 1 year after graduation about whether their medical school prepared them well, and compare responses with earlier cohorts. METHODS: We surveyed doctors who qualified in 2011 and 2012 from all UK medical schools. We obtained their responses to the statement 'My experience at medical school prepared me well for the jobs I have undertaken so far' on a 5-point scale from 'Strongly Agree' to 'Strongly Disagree'. Responses were compared with those of the UK graduates of 1999, 2000, 2002, 2005, 2008 and 2009, surveyed in the same way 1 year after graduation. RESULTS: The percentage of doctors who either 'Agreed' or 'Strongly Agreed' that they were well prepared doubled from 35% in 1999 to 70% in 2012, while the percentage who 'Strongly Agreed' with the statement increased fourfold. Perceptions of being well prepared have increased in graduates from almost every medical school. Variation between medical schools in self-reported preparedness of their graduates has decreased in recent cohorts. However, some large differences between medical schools remain. Significant differences in perceived preparedness remain between white and non-white doctors, but have diminished between men and women. CONCLUSIONS: Our work contributes to growing evidence suggesting that changes to medical education in the UK are producing doctors who feel well prepared for the challenges of being a doctor, though further improvements could be made.

The lyme disease pathogen has no effect on the survival of its rodent reservoir host.

Zoonotic pathogens that cause devastating morbidity and mortality in humans may be relatively harmless in their natural reservoir hosts. The tick-borne bacterium Borrelia burgdorferi causes Lyme disease in humans but few studies have investigated whether this pathogen reduces the fitness of its reservoir hosts under natural conditions. We analyzed four years of capture-mark-recapture (CMR) data on a population of white-footed mice, Peromyscus leucopus, to test whether B. burgdorferi and its tick vector affect the survival of this important reservoir host. We used a multi-state CMR approach to model mouse survival and mouse infection rates as a function of a variety of ecologically relevant explanatory factors. We found no effect of B. burgdorferi infection or tick burden on the survival of P. leucopus. Our estimates of the probability of infection varied by an order of magnitude (0.051 to 0.535) and were consistent with our understanding of Lyme disease in the Northeastern United States. B. burgdorferi establishes a chronic avirulent infection in their rodent reservoir hosts because this pathogen depends on rodent mobility to achieve transmission to its sedentary tick vector. The estimates of B. burgdorferi infection risk will facilitate future theoretical studies on the epidemiology of Lyme disease.

A multievent approach to estimating pair fidelity and heterogeneity in state transitions.

Fidelity rates of pair-bonded individuals are of considerable interest to behavioral and population biologists as they can influence population structure, mating rates, population productivity, and gene flow. Estimates of fidelity rates calculated from direct observations of pairs in consecutive breeding seasons may be biased because (i) individuals that are not seen are assumed to be dead, (ii) variation in the detectability of individuals is ignored, and (iii) pair status must be known with certainty. This can lead to a high proportion of observations being ignored. This approach also restricts the way variation in fidelity rates for different types of individuals, or the covariation between fidelity and other vital rates (e.g., survival) can be analyzed. In this study, we develop a probabilistic multievent capture-mark-recapture (MECMR) modeling framework for estimating pair fidelity rates that accounts for imperfect detection rates and capture heterogeneity, explicitly incorporates uncertainty in the assessment of pair status, and allows estimates of state-dependent survival and fidelity rates to be obtained simultaneously. We demonstrate the utility of our approach for investigating patterns of fidelity in pair-bonded individuals, by applying it to 30 years of breeding data from a wild population of great tits Parus major Linnaeus. Results of model selection supported state-dependent recapture, survival, and fidelity rates. Recapture rates were higher for individuals breeding with their previous partner than for those breeding with a different partner. Faithful birds that were breeding with the same partner as in the previous breeding season (i.e., at t - 1) experienced substantially higher survival rates (between t and t + 1) and were also more likely to remain faithful to their current partner (i.e., to remain in the faithful state at t + 1). First year breeders were more likely to change partner than older birds. These findings imply that traditional estimates, which do not account for state-dependent parameters, may be both inaccurate and biased, and hence, inferences based on them may conceal important biological effects. This was demonstrated in the analysis of simulated capture histories, which showed that our MECMR model was able to estimate state-dependant survival and pair fidelity rates in the face of varying state-dependant recapture rates robustly, and more accurately, than the traditional method. In addition, this new modeling approach provides a statistically rigorous framework for testing hypothesis about the causes and consequences of fidelity to a partner for natural populations. The novel modeling approach described here can readily be applied, either in its current form or via extension, to other populations and other types of dyadic interactions (e.g., between nonpaired individuals, such as parent-offspring relationships, or between individuals and locations, such as nest-site fidelity).

Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population.

Major histocompatibility complex (Mhc) genes are believed to play a key role in the genetic basis of disease control. Although numerous studies have sought links between Mhc and disease prevalence, many have ignored the ecological and epidemiological aspects of the host-parasite interaction. Consequently, interpreting associations between prevalence and Mhc has been difficult, whereas discriminating alleles for qualitative resistance, quantitative resistance and susceptibility remains challenging. Moreover, most studies to date have quantified associations between genotypes and disease status, overlooking the complex relationship between genotype and the properties of the Mhc molecule that interacts with parasites. Here, we address these problems and demonstrate avian malaria (Plasmodium) parasite species-specific associations with functional properties of Mhc molecules (Mhc supertypes) in a wild great tit (Parus major) population. We further show that correctly interpreting these associations depends crucially on understanding the spatial variation in risk of infection and the fitness effects of infection. We report that a single Mhc supertype confers qualitative resistance to Plasmodium relictum, whereas a different Mhc supertype confers quantitative resistance to Plasmodium circumflexum infections. Furthermore, we demonstrate common functional properties of Plasmodium-resistance alleles in passerine birds, suggesting this is a model system for parasite-Mhc associations in the wild.

Mhc-linked survival and lifetime reproductive success in a wild population of great tits.

Major histocompatibility complex (Mhc) genes are frequently used as a model for adaptive genetic diversity. Although associations between Mhc and disease resistance are frequently documented, little is known about the fitness consequences of Mhc variation in wild populations. Further, most work to date has involved testing associations between Mhc genotypes and fitness components. However, the functional diversity of the Mhc, and hence the mechanism by which selection on Mhc acts, depends on how genotypes map to the functional properties of Mhc molecules. Here, we test three hypotheses that relate Mhc diversity to fitness: (i) the maximal diversity hypothesis, (ii) the optimal diversity hypothesis and (iii) effect of specific Mhc types. We combine mark-recapture methods with analysis of long-term breeding data to investigate the effects of Mhc class I functional diversity (Mhc supertypes) on individual fitness in a wild great tit (Parus major) population. We found that the presence of three different Mhc supertypes was associated with three different components of individual fitness: survival, annual recruitment and lifetime reproductive success (LRS). Great tits possessing Mhc supertype 3 experienced higher survival rates than those that did not, whereas individuals with Mhc supertype 6 experienced higher LRS and were more likely to recruit offspring each year. Conversely, great tits that possessed Mhc supertype 5 had reduced LRS. We found no evidence for a selective advantage of Mhc diversity, in terms of either maximal or optimal supertype diversity. Our results support the suggestion that specific Mhc types are an important determinant of individual fitness.

Epidemiology of the emergent disease Paridae pox in an intensively studied wild bird population.

Paridae pox, a novel avipoxvirus infection, has recently been identified as an emerging infectious disease affecting wild tit species in Great Britain. The incursion of Paridae pox to a long-term study site where populations of wild tits have been monitored in detail for several decades provided a unique opportunity to obtain information on the local-scale epidemiological characteristics of this novel infection during a disease outbreak. Using captures of >8000 individual birds, we show that, within two years of initial emergence, Paridae pox had become established within the population of great tits (Parus major) reaching relatively high peak prevalence (10%), but was far less prevalent (<1%) in sympatric populations of several other closely related, abundant Paridae species. Nonlinear smoothing models revealed that the temporal pattern of prevalence among great tits was characterised by within-year fluctuations indicative of seasonal forcing of infection rates, which was likely driven by multiple environmental and demographic factors. There was individual heterogeneity in the course of infection and, although recovery was possible, diseased individuals were far less likely to be recaptured than healthy individuals, suggesting a survival cost of infection. This study demonstrates the value of long-term monitoring for obtaining key epidemiological data necessary to understand disease dynamics, spread and persistence in natural populations.

Emergence of a novel avian pox disease in British tit species.

Avian pox is a viral disease with a wide host range. In Great Britain, avian pox in birds of the Paridae family was first diagnosed in a great tit (Parus major) from south-east England in 2006. An increasing number of avian pox incidents in Paridae have been reported each year since, indicative of an emergent infection. Here, we utilise a database of opportunistic reports of garden bird mortality and morbidity to analyse spatial and temporal patterns of suspected avian pox throughout Great Britain, 2006-2010. Reports of affected Paridae (211 incidents) outnumbered reports in non-Paridae (91 incidents). The majority (90%) of Paridae incidents involved great tits. Paridae pox incidents were more likely to involve multiple individuals (77.3%) than were incidents in non-Paridae hosts (31.9%). Unlike the small wart-like lesions usually seen in non-Paridae with avian pox in Great Britain, lesions in Paridae were frequently large, often with an ulcerated surface and caseous core. Spatial analyses revealed strong clustering of suspected avian pox incidents involving Paridae hosts, but only weak, inconsistent clustering of incidents involving non-Paridae hosts. There was no spatial association between Paridae and non-Paridae incidents. We documented significant spatial spread of Paridae pox from an origin in south-east England; no spatial spread was evident for non-Paridae pox. For both host clades, there was an annual peak of reports in August/September. Sequencing of the avian poxvirus 4b core protein produced an identical viral sequence from each of 20 great tits tested from Great Britain. This sequence was identical to that from great tits from central Europe and Scandinavia. In contrast, sequence variation was evident amongst virus tested from 17 non-Paridae hosts of 5 species. Our findings show Paridae pox to be an emerging infectious disease in wild birds in Great Britain, apparently originating from viral incursion from central Europe or Scandinavia.

Individual and population-level impacts of an emerging poxvirus disease in a wild population of great tits.

Emerging infectious diseases of wildlife can have severe effects on host populations and constitute a pressing problem for biodiversity conservation. Paridae pox is an unusually severe form of avipoxvirus infection that has recently been identified as an emerging infectious disease particularly affecting an abundant songbird, the great tit (Parus major), in Great Britain. In this study, we study the invasion and establishment of Paridae pox in a long-term monitored population of wild great tits to (i) quantify the impact of this novel pathogen on host fitness and (ii) determine the potential threat it poses to population persistence. We show that Paridae pox significantly reduces the reproductive output of great tits by reducing the ability of parents to fledge young successfully and rear those young to independence. Our results also suggested that pathogen transmission from diseased parents to their offspring was possible, and that disease entails severe mortality costs for affected chicks. Application of multistate mark-recapture modelling showed that Paridae pox causes significant reductions to host survival, with particularly large effects observed for juvenile survival. Using an age-structured population model, we demonstrate that Paridae pox has the potential to reduce population growth rate, primarily through negative impacts on host survival rates. However, at currently observed prevalence, significant disease-induced population decline seems unlikely, although pox prevalence may be underestimated if capture probability of diseased individuals is low. Despite this, because pox-affected model populations exhibited lower average growth rates, this emerging infectious disease has the potential to reduce the resilience of populations to other environmental factors that reduce population size.

Reduced effect of Tasmanian devil facial tumor disease at the disease front.

Pathogen-driven declines in animal populations are increasingly regarded as a major conservation issue. The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction by devil facial tumor disease, a unique transmissible cancer. The disease is transmitted through direct transfer of tumor cells, which is possible because the genetic diversity of Tasmanian devils is low, particularly in the major histocompatibility complex genes of the immune system. The far northwest of Tasmania now holds the last remaining disease-free wild devil populations. The recent discovery of unique major histocompatibility complex genotypes in the northwestern region of Tasmania has raised the possibility that some animals may be resilient to the disease. We examined the differences in the epidemiology and population effects of devil facial tumor disease at 3 well-studied affected sites in eastern Tasmania and 1 in western Tasmania (West Pencil Pine). In contrast to the 3 eastern sites, there has been no rapid increase in disease prevalence or evidence of population decline at West Pencil Pine. Moreover, this is the only onsite at which the population age structure has remained unaltered 4 years after the first detection of disease. The most plausible explanations for the substantial differences in population effects and epidemiology of the disease between eastern and western sites are geographic differences in genotypes or phenotypes of devils and functional differences between tumor strains in the 2 regions. We suggest that conservation efforts focus on identifying whether either or both these explanations are correct and then, if resistance alleles exist, to attempt to spread the resistant alleles into affected populations. Such assisted selection has rarely been attempted for the management of wildlife diseases, but it may be widely applicable.

Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates.

1. Investigating the ecological context in which host-parasite interactions occur and the roles of biotic and abiotic factors in forcing infection dynamics is essential to understanding disease transmission, spread and maintenance. 2. Despite their prominence as model host-pathogen systems, the relative influence of environmental heterogeneity and host characteristics in influencing the infection dynamics of avian blood parasites has rarely been assessed in the wild, particularly at a within-population scale. 3. We used a novel multievent modelling framework (an extension of multistate mark-recapture modelling) that allows for uncertainty in disease state, to estimate transmission parameters and assess variation in the infection dynamics of avian malaria in a large, longitudinally sampled data set of breeding blue tits infected with two divergent species of Plasmodium parasites. 4. We found striking temporal and spatial heterogeneity in the disease incidence rate and the likelihood of recovery within this single population and demonstrate marked differences in the relative influence of environmental and host factors in forcing the infection dynamics of the two Plasmodium species. 5. Proximity to a permanent water source greatly influenced the transmission rates of P. circumflexum, but not of P. relictum, suggesting that these parasites are transmitted by different vectors. 6. Host characteristics (age/sex) were found to influence infection rates but not recovery rates, and their influence on infection rates was also dependent on parasite species: P. relictum infection rates varied with host age, whilst P. circumflexum infection rates varied with host sex. 7. Our analyses reveal that transmission of endemic avian malaria is a result of complex interactions between biotic and abiotic components that can operate on small spatial scales and demonstrate that knowledge of the drivers of spatial and temporal heterogeneity in disease transmission will be crucial for developing accurate epidemiological models and a thorough understanding of the evolutionary implications of pathogens.

Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure.

1. Parasites can have important effects on host populations influencing either fecundity or mortality, but understanding the magnitude of these effects in endemic host-parasite systems is challenging and requires an understanding of ecological processes affecting both host and parasite. 2. Avian blood parasites (Haemoproteus and Plasmodium) have been much studied, but the effects of these parasites on hosts in areas where they are endemic remains poorly known. 3. We used a multistate modelling framework to explore the effects of chronic infection with Plasmodium on survival and recapture probability in a large data set of breeding blue tits, involving 3424 individuals and 3118 infection diagnoses over nine years. 4. We reveal strong associations between chronic malaria infection and both recapture and survival, effects that are dependent on the clade of parasite, on host traits and on the local risk of infection. 5. Infection with Plasmodium relictum was associated with reduced recapture probability and increased survival, compared to P. circumflexum, suggesting that these parasites have differing virulence and cause different types of selection on this host. 6. Our results suggest a large potential survival cost of acute infections revealed by modelling host survival as a function of the local risk of infection. 7. Our analyses suggest not only that endemic avian malaria may have multiple fitness effects on their hosts and that these effects are species dependent, but also that adding ecological structure (in this case parasite species and spatial variation in disease occurrence) to analyses of host-parasite interactions is an important step in understanding the ecology and evolution of these systems.